Sociodemographic inequalities in cardiovascular risk factors among adolescents from indigenous areas in Chiapas, Mexico

Abstract: This study was aimed to determine the prevalence of cardiovascular risk factors among different sociodemographic groups of adolescents from indigenous communities in Chiapas, Mexico. A cross-sectional prevalence study was performed in urban and rural communities in the Tzotzil-Tzeltal and Selva regions of Chiapas. A sample of 253 adolescents was studied, of whom 48% were girls and 52% were boys. A descriptive analysis of quantitative variables was performed using measures of central tendency and dispersion. The prevalence of cardiovascular risk factors stratified by sex, geographical area, years of schooling, and ethnicity of the mothers was estimated. The prevalence of cardiovascular risk factors was analyzed in relation to the sociodemographic characteristics of the study population. Low HDL-c (51%) was the predominant cardiovascular risk factor. Girls had a higher prevalence of abdominal obesity, hypertriglyceridemia, and borderline total cholesterol than boys. High diastolic blood pressure was more prevalent in boys. Adolescents from urban areas had a higher prevalence of overweight/obesity and insulin resistance than adolescents from rural areas. The prevalence of overweight/obesity and abdominal obesity was higher in adolescents whose mothers had ≥ 7 years of schooling compared with adolescents with less educated mothers. Differences by maternal ethnicity also influenced the prevalence of insulin resistance. Among the main findings, this study associated sociodemographic and geographical inequalities with cardiovascular risk factors. Promoting a healthy lifestyle for this young population is absolutely necessary to prevent cardiovascular diseases in adulthood.


Introduction
In recent decades, interest in the study of health inequalities has grown.According to previous evidence, in Mexico, certain chronic and infectious diseases, such as malnutrition, tuberculosis 1 , anemia, cervical cancer, metabolic syndrome, and diabetes 2 , were more frequent among individuals of low socioeconomic status.In Mexico, cardiovascular diseases (CVD) are the main cause of mortality, representing an important public health problem.Evidence shows the association of different risk factors with CVD.Abnormal lipid metabolism during childhood 3 is a risk factor for atheromatous plaques during adulthood 4 .Changes in other metabolic risk factors, such as serum glucose, insulin, C-reactive protein 5 , blood pressure, and waist circumference, are also associated with an increased risk of CVD 6 .
In Latin American countries such as Brazil, Chile, and Venezuela, obesity and dyslipidemia are highly prevalent 7 .A study with 180 adolescents from Mexico City showed that 61% had hypertriglyceridemia and half of them had low concentrations of high-density lipoprotein cholesterol (HDL-c) 8 .In the State of Morelos, a study with 869 adolescents found that 7% had metabolic syndrome, 68% hypertriglyceridemia, 17% low HDL-c, and 15% hyperglycemia 9 .In the city of Tuxtla Gutiérrez, Chiapas, the prevalence of metabolic syndrome in adolescents was 16% 10 .However, studies conducted in other countries have shown that cardiovascular risk can be influenced by socioeconomic status 11 , ethnicity 12,13 , and geographical area 14 .In Mexico, few studies compare cardiovascular risk factors between indigenous peoples and the general population.A study performed with adolescents from urban and rural schools in Central Mexico showed a high prevalence of hypoalphalipoproteinemia, especially among boys from the rural area, where the main ethnic groups were the Mazahuas and the Otomi 15 .Another study with adults in Chiapas showed that the mestizo population had a higher risk of CVD than the indigenous population 16 .To date, the specialized literature presents little evidence on cardiovascular risk factors for adolescents in Chiapas.Thus, this study aims to measure the prevalence of cardiovascular risk factors and analyze their distribution among different population groups in Chiapas.

Study and sample design
This cross-sectional prevalence study was conducted with a sample of adolescents from a birth cohort study, born in three public hospitals in Chiapas in 2003.The sampling had two stages.In the first stage, the communities to which adolescents belong were clustered according to population size and geographical area (rural/urban).In the second stage, a systematic sampling of adolescents was performed with a randomized start-up 17 .

Study population
In total, 303 adolescents of both sexes, with a mean age of 14.1 years, from 14 municipalities in the Tzotzil-Tzeltal and Selva regions of Chiapas were selected 17 .Of them, 50, without biochemical data, were excluded, obtaining a final sample of 253 adolescents.

Survey information
Interviews were conducted with adolescents and their mothers or caregivers at their homes.A precoded and structured questionnaire was applied, covering the following information: sociodemographic data, non-pathological personal history, family medical history, anthropometric and clinical measurements.Blood samples were collected for biochemical analyses.Sociodemographic data included sex, age, geographical area (rural/urban), ethnicity, and years of schooling of adolescents and their mothers, and household assets.Family medical history included diseases of first-and second-Cad.Saúde Pública 2023; 39(11):e00024623 degree relatives and non-pathological personal history (smoking and alcohol use).The anthropometric and clinical assessment considered weight, height, waist circumference, and blood pressure.

Data collection procedures
Data were collected by a multidisciplinary fieldwork team (medicine, biology, clinical chemistry, and nutrition) 17 .Weight was measured by electronic scales (accuracy ± 100g, Model UM081, Tanita Corporation, https://www.tanita.com/es/).Height was measured using stadiometers (accuracy ± 1mm, SECA, https://www.seca.com/de_de.html).Body mass index (BMI) was estimated by dividing weight by height squared and BMI z-score was calculated with AnthroPlus v. 1.0.4(https://who-anthroplus. freedownloadscenter.com/windows/).As the main interest of this study is overweight/obesity as a risk factor, nutritional status was classified as normal weight [< 1 standard deviation (SD)] and overweight/obesity [BMI z-score ≥ 1 SD].Waist circumference was measured by anthropometric tapes (accuracy ± 1mm, SECA).The cut-off point for abdominal obesity was ≥ 80cm in girls and ≥ 90cm in boys, according to the International Diabetes Federation 18 .
Blood pressure was measured twice on the right mid-arm using a digital monitor (Model CH-453, Citizen, https://www.citizen-systems.co.jp/english/support/index.html) while the adolescent was sitting and after a five-minute rest.Systolic blood pressure (SBP) and diastolic blood pressure (DBP) were classified as normal (< 90th percentile) or high (≥ 90th percentile) 19 , using the percentile tables of the US National Institutes of Health for age, sex, and height 20 .

• Insulin resistance
The homeostatic model to assess insulin resistance (HOMA-IR) was estimated by multiplying fasting blood glucose (mg/dL) by fasting insulin (µU/mL) divided by 22.5.The cut-off point used to determine insulin resistance was 2.97 22 .

• Cardiovascular risk
To discriminate cardiovascular risk by hs-CRP, the following cut-off points of the US Centers for Disease Control and Prevention (CDC) and the American Heart Association (AHA) were used: low risk hs-CRP < 1mg/dL, average risk 1-3mg/dL, and high risk > 3mg/dL 23 .

• Metabolic syndrome
The diagnosis of metabolic syndrome was analyzed according to the criteria of the National Cholesterol Education Program Adult Treatment Panel III (NCEP-ATP III), previously used by Ford et al. 19 .According to NCEP-ATP III definition, the diagnosis of metabolic syndrome must include three or more of the following factors (for both sexes): abdominal obesity (waist circumference ≥ 90th sexspecific percentile), triglycerides ≥ 110mg/dL, HDL-c ≤ 40mg/dL, SBP or DBP ≥ 90th percentile (age-, height-, and sex-specific), and glucose ≥ 110mg/dL 24 .

Statistical analysis
A descriptive analysis of quantitative variables was performed using measures of central tendency and dispersion.The prevalence of cardiovascular risk factors and 95% confidence intervals (95%CI) were estimated, stratified by sex, geographical area (rural/urban), years of schooling, and maternal ethnicity.The difference between variable distributions was obtained by Mann-Whitney U tests (for nonparametric variables) and independent samples t-tests (for parametric variables).The proportions of qualitative variables were analyzed using the Bonferroni correction.All analyses were performed in SPSS (https://www.ibm.com/).

Ethical approval and participation consent
Before the interview, mothers or caregivers and adolescents signed an informed consent form.This study was approved by the Research Ethics Committee of the El Colegio de la Frontera Sur (CEI-O-076/16).

Results
Of the 253 adolescents, 52% were boys and 75% lived in urban areas.Table 1 presents the sociodemographic characteristics of adolescents according to sex.Their mean age was 14 years and their mean years of schooling was 6.5 years.In total, 46% of mothers spoke an indigenous language and 56.4% had < 7 years of schooling.Of adolescents' fathers, 30% had < 7 years of schooling and 53% spoke an indigenous language.Regarding household assets, 4% of participants had no running water, 32% cooked with charcoal/firewood, 12% had a latrine, septic tank, or none of them, 36% had no fridge, 13% had no television, 22% had no cell phone, and 80% had no computer.In total, 77% of adolescents ate red meat less than once per week and only 12% had medical insurance (Institute for Social Security and Services for State Workers -ISSSTE, Social Security Institute of Workers of the State of Chiapas -ISSSTECH, Mexican Social Security Institute -IMSS, Mexican Ministry of National Defense -SEDENA).We found differences in socioeconomic characteristics between the sexes in terms of having a fridge and cooking fuel (Table 1).
Table 2 shows the adolescents' family medical history and non-pathological personal history.Around 45% of adolescents had relatives with chronic diseases.The most commonly reported diseases were type 2 diabetes, hypertension, and CVD.In total, 68% followed the Mexican vaccination schedule, boys less than girls, and 54% were not exclusively breastfed in their first six months of life.Among the adolescents, 20% consumed alcohol occasionally, boys less than girls, and 16% had smoked at least once in their lives.
Table 3 shows the prevalence of cardiovascular risk factors by sex.The most prevalent risk factor was low HDL-c (51%), followed by borderline triglycerides (35%), overweight/obesity (29%), and hypertriglyceridemia (28%).A small percentage of the population had high LDL-c levels (1%), abnormal fasting blood glucose (3%), and high total cholesterol (4%).A significantly higher proportion of girls had abdominal obesity (p < 0.001), borderline total cholesterol (p = 0.002), and high triglycerides (p = 0.021) as compared with boys.Moreover, the prevalence of overweight/obesity was 45% higher in girls than in boys.However, boys presented greater prevalence of high DBP and low HDL-c levels.

Table 2
Family medical history and non-pathological personal history of adolescents *.Table 4 presents the prevalence of cardiovascular risk factors according to geographical area (urban/rural).In urban areas, the prevalence of overweight/obesity (33%) and insulin resistance (28%) was significantly higher compared with rural areas.Moreover, we found a borderline significant difference in abdominal obesity among adolescents living in urban areas (16.9%) compared with rural areas (7.8%).

Parameter
Regarding maternal schooling (Table 5), this study observed a significantly higher prevalence of overweight/obesity and abdominal obesity among adolescents whose mothers had ≥ 7 years of schooling.On the other hand, adolescents with mothers with < 7 years of schooling had a higher prevalence of low HDL-c.Regarding maternal ethnicity (Table 6), adolescents whose mothers did not speak an indigenous language had a significantly higher prevalence of insulin resistance compared with adolescents whose mothers spoke an indigenous language (HOMA-IR ≥ 2.97 units).Moreover, the prevalence of low HDL-c was higher among adolescents whose mothers spoke an indigenous language (56.3%) compared with adolescents whose mothers spoke only Spanish (45%).
Table 7 shows the prevalence of metabolic syndrome defined by the NCEP-ATP III criteria, according to different populations.According to the NCEP-ATP, the prevalence of metabolic syndrome was 14.6%.This prevalence was higher in girls, urban areas, and adolescents with mothers who spoke an indigenous language and had ≥ 7 years of schooling.

Discussion
This study found a high prevalence of cardiovascular risk factors, such as overweight/obesity, low HDL-c, high triglycerides, and insulin resistance, among adolescents from 58 mestizo and indigenous communities in two regions of Chiapas.The prevalence of overweight/obesity in the study population was 29%, higher in urban areas (32.8%) than in rural areas (17.2%).Similarly, the Mexican National Survey of Health and Nutrition (ENSANUT 2016) for adolescents aged 12 to 19 years showed that the prevalence of overweight/obesity in urban areas was slightly higher (36.7%) than in rural areas (35%).The high prevalence of overweight/obesity found in this age group in our study is remarkable.This finding may be the result of the nutritional transition and lifestyle changes observed over the last decades, especially in urban areas.In these areas, the Mexican population has become sedentary 2 and has been exposed to Westernized dietary patterns, characterized by energy-dense, nutrient-poor foods and sugar-sweetened beverages 25 .Moreover, the population in this study had a double burden of malnutrition, as in a previous study by the same authors, with a high prevalence of stunting among adolescents in rural areas 17 .The prevalence of overweight/obesity and abdominal obesity was higher in adolescents whose mothers had ≥ 7 years of schooling.A study with schoolchildren in the state of Guerrero, Mexico, found that maternal schooling increased the likelihood of overweight among their children 26 .Another study conducted in three Mexican cities (Tijuana, Tuxtla Gutiérrez, and Reynosa) also showed that among children from low-income families whose mothers had higher schooling levels, the prevalence of overweight/obesity was higher 27 .In this study, the prevalence of abdominal obesity was 14.6%.We found differences by sex, as girls had the highest prevalence of abdominal obesity (24.6%).The relationship between abdominal obesity and sex in adolescents is still controversial.For example, previous studies in Spain 28   Brazil 29 showed a higher prevalence of abdominal obesity in boys than in girls.This may be due to the difference in total body fat between the sexes, considering the higher percentage of body fat in girls and the redistribution of fat from the extremities to the trunk.This distribution differs between the sexes, since changes in body fat are associated with estrogen and testosterone levels 30 .Disparities between the sexes can also be attributed to social and cultural differences.In Mexico, the prevalence of overweight in girls increased from 23.7% in 2012 to 26.4% in 2016, while in boys, the prevalence remained unchanged 31 .In Chiapas, the prevalence of overweight/obesity in girls also increased from 30.7% in 2006 to 32.1% in 2012 32 .
Regarding blood pressure, in our study, the proportion of boys with DBP ≥ 90th percentile was higher than the proportion of girls.A previous study with adolescents in the United States also showed that, after the onset of puberty, boys had higher blood pressure than girls of the same age 33 .The mechanisms responsible for the differences in blood pressure during adolescence between the sexes are still unclear.Evidence shows that androgens, such as testosterone, may play an important role in regulating blood pressure in sex-related differences 34 , since testosterone levels cause endothelial dysfunction 35 .
Our findings for blood lipids, stratified by sex, showed that triglycerides and borderline total cholesterol were higher in girls than in boys.These differences by sex can be explained by the different hormonal activity during adolescence 36 .The girls in our study had higher waist circumference values, which may explain their higher triglycerides levels.The most prevalent risk factor found in rural areas was high triglycerides levels, although this difference compared with urban areas was not statistically significant.This result is in line with a study with adolescents from Mexico City and a rural community in Central Mexico, where 45% of the population is predominantly Mazahua and Otomi 37 .This finding can be partly explained by dietary intake.Low-fat and high-carbohydrate diets Cad.Saúde Pública 2023; 39(11):e00024623

Table 6
Prevalence of cardiovascular risk factors in adolescents according to their mother's language.increase triglyceride levels 38 .In our study, the mean carbohydrate intake was 356g per day in rural areas and 322g in urban areas.These values are higher than the average for Mexican adolescents in rural areas (285g per day for girls and 326g for boys).Moreover, 69% of girls and 61% of boys in rural areas regularly consume an excess of added sugars 39 .The prevalence of borderline total cholesterol was higher in girls (14.8%) than in boys (3.8%), but we found no differences by geographic area.A study reports that total cholesterol levels decrease in boys in early puberty, but increase again as they approach adulthood.In contrast, total cholesterol levels increase during puberty in girls 40 .However, as we did not measure Tanner stages, we could not differentiate sexual maturation, which could influence our results.

Cardiovascular risk factors
Regarding HDL-c levels, we found a higher prevalence of low HDL-c in adolescents whose mothers had < 7 years of schooling compared with adolescents with mothers with ≥ 7 years of schooling.In line with our results, a previous study showed a trend towards a higher prevalence of low HDL-c in Mexican adults with lower socioeconomic status and schooling level 41 .Moreover, we found a borderline significant difference in the prevalence of low HDL-c.Low HDL-c was higher among adolescents whose mothers spoke an indigenous language compared with adolescents whose mothers spoke only Spanish.Ethnic disparities in HDL-c levels may result from the presence and interaction of multiple components, such as genotype, body composition, lifestyle habits, and perceptions 42 .For example, regarding genotype, the C230 variant of ATP-binding cassette transporter A1 (ABCA1) was associated with an increased risk of hypoalphalipoproteinemia in Mexican children 43 and adults 44 .Among the Mayan population, the frequency of the C230 allelic variant (0.288) was higher than in the Mexican mestizo population (0.109) 45 .The presence of this allelic variant translates directly into a 30% reduction in the ABCA1 transporter, which is heavily involved in HDL biogenesis 46 .However, we highlight that the population-attributable risk of hypoalphalipoproteinemia from the C230 allele of ABCA1 in Mexico is around 12% 44 .Thus, ethnic disparities in low HDL-c levels should not be attributed only to genetic factors, since other factors may be involved, such as behavioral (poor diet), cultural, and linguistic barriers, socioeconomic disparities 47 , or unequal access to health care and facilities 12 .
The prevalence of insulin resistance in this study was considerably high (24%).We also found that insulin resistance in urban areas was higher than in rural areas.This finding is in line with previous studies, in which the urban environment was an independent predictor of insulin resistance 48 .Evidence shows that insulin resistance is associated with lipid changes in early life and with overweight/ obesity 49 .Thus, the interaction between the high prevalence of obesity and changes in lipid metabolism in our sample may also explain our results.Moreover, the prevalence of insulin resistance was higher in adolescents whose mothers were not indigenous.In Chiapas, most rural population is indigenous 50 .We found no differences in HOMA-IR between the sexes and regarding maternal schooling.
The analysis of hs-CRP showed that 25% of adolescents had moderate and high cardiovascular risk according to CDC and AHA, with higher hs-CRP levels in girls, urban areas, and adolescents with less educated mothers, despite the lack of statistically significant differences.Similar to our results, a study with 418 Mexican adolescents from the city of Guadalajara showed no differences in cardiovascular risk regarding hs-CRP between the sexes 51 .
Regarding metabolic syndrome in the study population, results showed a high prevalence (14.6%) according to the NCEP-ATP III criteria.Other studies conducted in Mexico showed a different prevalence: 8.8% at national level 52 , 6.7% in Morelos 9 , and 20% in Campeche 53 , which has the highest prevalence of diabetes and hypertension in the country.
The nutritional transition in the population of Chiapas may be among the possible explanations for the situation found in our study 54 .In recent decades, dietary patterns have shifted from a traditional plant-based diet to a Westernized eating style consisting of a high fat and refined carbohydrate intake 55 .ENSANUT 2016 showed that adolescents habitually consumed food groups not recommended for daily consumption: 84% habitually consumed sugary drinks, 59% snacks, sweets, and desserts, and 50% sweetened cereals 31 .
Sedentary behavior among adolescents has also been associated with insulin resistance, lipid changes, and higher inflammatory states 56 .The adolescents studied spent 10 hours per day sitting (nine hours for the rural population) and only one hour and 40 minutes per week exercising or practicing sports, without differences between the sexes.
Cad. Saúde Pública 2023; 39 (11):e00024623 Socioeconomic factors and mechanisms such as different access to food, schooling level, health services, information, income, occupation, and empowerment can explain the disparities found between populations and geographical areas.One of the main strengths of this study is that it documents sociodemographic inequalities in cardiovascular risk factors among adolescents from marginalized Mayan communities in Chiapas, which have been little studied previously.This allowed us to identify vulnerable groups in order to develop future, precise interventions to modify their cardiovascular risk profiles.Every individual of the sample studied received their results in private, along with nutritional counseling.
This study with adolescents from marginalized indigenous areas in Chiapas showed sociodemographic and geographical disparities in cardiovascular risk factors.Girls had a higher prevalence of risk factors.We found a differential pattern of risk factors regarding geographical area, as the urban population was more vulnerable to overweight/obesity, while the rural population was more vulnerable to low HDL-c levels.
Based on these results, we recommend the creation of effective and targeted public health policies to improve the well-being of adolescents from marginalized indigenous areas: (1) monitoring nutritional status and promoting healthy lifestyles; (2) preventing and controlling the increasing prevalence of cardiovascular risk factors in the study population; (3) creating social and economic interventions to improve living conditions and prevent chronic diseases in adulthood; (4) continuing health surveillance in the studied population; (5) implementing culturally adapted models to bring health care to rural areas; and (6) conducting further studies on the genetic determinants of CVD in ethnic minorities.

Table 1
Sociodemographic characteristics of the sample of adolescents by sex *.

Table 1 (continued)
ISSSTE: Institute for Social Security and Services for State Workers; ISSSTECH: Social Security Institute of Workers of the State of Chiapas; IMSS: Mexican Social Security Institute; SD: standard deviation; SEDENA: Mexican Ministry of National Defense.

Table 3
Prevalence of cardiovascular risk factors in adolescents according to sex.

Table 4
Prevalence of cardiovascular risk factors in adolescents according to geographical area.

Table 5
Prevalence of cardiovascular risk factors in adolescents according to their mother's schooling.

Table 7
Prevalence of metabolic syndrome among adolescents from different sociodemographic groups and geographical areas.